Spectral fingerprints of large‐scale cortical dynamics during ambiguous motion perception

Ambiguous stimuli have been widely used to study the neuronal correlates of consciousness. Recently, it has been suggested that conscious perception might arise from the dynamic interplay of functionally specialized but widely distributed cortical areas. While previous research mainly focused on phase coupling as a correlate of cortical communication, more recent findings indicated that additional coupling modes might coexist and possibly subserve distinct cortical functions. Here, we studied two coupling modes, namely phase and envelope coupling, which might differ in their origins, putative functions and dynamics. Therefore, we recorded 128‐channel EEG while participants performed a bistable motion task and utilized state‐of‐the‐art source‐space connectivity analysis techniques to study the functional relevance of different coupling modes for cortical communication. Our results indicate that gamma‐band phase coupling in extrastriate visual cortex might mediate the integration of visual tokens into a moving stimulus during ambiguous visual stimulation. Furthermore, our results suggest that long‐range fronto‐occipital gamma‐band envelope coupling sustains the horizontal percept during ambiguous motion perception. Additionally, our results support the idea that local parieto‐occipital alpha‐band phase coupling controls the inter‐hemispheric information transfer. These findings provide correlative evidence for the notion that synchronized oscillatory brain activity reflects the processing of sensory input as well as the information integration across several spatiotemporal scales. The results indicate that distinct coupling modes are involved in different cortical computations and that the rich spatiotemporal correlation structure of the brain might constitute the functional architecture for cortical processing and specific multi‐site communication. Hum Brain Mapp 37:4099–4111, 2016. © 2016 Wiley Periodicals, Inc.

[1]  Niels A. Kloosterman,et al.  Pupil size tracks perceptual content and surprise , 2015, The European journal of neuroscience.

[2]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[3]  Daniel Strüber,et al.  MEG alpha activity decrease reflects destabilization of multistable percepts. , 2002, Brain research. Cognitive brain research.

[4]  F. Tong,et al.  Neural mechanisms of object-based attention. , 2015, Cerebral cortex.

[5]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[6]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[7]  M. Siegel,et al.  Dissociating neuronal gamma-band activity from cranial and ocular muscle activity in EEG , 2013, Front. Hum. Neurosci..

[8]  Barbara F. Händel,et al.  Cross-frequency coupling of brain oscillations indicates the success in visual motion discrimination , 2009, NeuroImage.

[9]  D. Glaser,et al.  Metastable motion anisotropy , 1991, Visual Neuroscience.

[10]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[11]  Andreas Bartels,et al.  Binocular rivalry: a time dependence of eye and stimulus contributions. , 2010, Journal of vision.

[12]  Peter Dechent,et al.  Transcranial alternating current stimulation affects the BOLD signal in a frequency and task‐dependent manner , 2015, Human brain mapping.

[13]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[14]  Philipp Sterzer,et al.  A neural basis for inference in perceptual ambiguity , 2007, Proceedings of the National Academy of Sciences.

[15]  Michael Rose,et al.  Brief Report: Altered Horizontal Binding of Single Dots to Coherent Motion in Autism , 2010, Journal of autism and developmental disorders.

[16]  P. König,et al.  Combining EEG and eye tracking: identification, characterization, and correction of eye movement artifacts in electroencephalographic data , 2012, Front. Hum. Neurosci..

[17]  Bart Gips,et al.  Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing , 2014, Trends in Neurosciences.

[18]  M. Siegel,et al.  A framework for local cortical oscillation patterns , 2011, Trends in Cognitive Sciences.

[19]  J. Schoffelen,et al.  Nonparametric statistical testing of coherence differences , 2007, Journal of Neuroscience Methods.

[20]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[21]  Y. Nakayama,et al.  Memorial message for the 10th anniversary of journal of visualization , 2007, J. Vis..

[22]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[23]  R. S. J. Frackowiak,et al.  Human brain activity during spontaneously reversing perception of ambiguous figures , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[25]  Michael Bach,et al.  Ambiguous Figures – What Happens in the Brain When Perception Changes But Not the Stimulus , 2011, Front. Hum. Neurosci..

[26]  E Başar,et al.  Frontal gamma-band enhancement during multistable visual perception. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  Philipp Sterzer,et al.  A neural signature of colour and luminance correspondence in bistable apparent motion , 2005, The European journal of neuroscience.

[28]  T. Ergenoğlu,et al.  DRD4 and DAT1 polymorphisms modulate human gamma band responses. , 2007, Cerebral cortex.

[29]  R. Blake,et al.  Negligible fronto-parietal BOLD activity accompanying unreportable switches in bistable perception , 2015, Nature Neuroscience.

[30]  N. Logothetis,et al.  Multistable phenomena: changing views in perception , 1999, Trends in Cognitive Sciences.

[31]  N. Logothetis,et al.  Disrupting Parietal Function Prolongs Dominance Durations in Binocular Rivalry , 2010, Current Biology.

[32]  A. Engel,et al.  Intrinsic Coupling Modes: Multiscale Interactions in Ongoing Brain Activity , 2013, Neuron.

[33]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[34]  Pascal Fries,et al.  Communication through coherence with inter-areal delays , 2015, Current Opinion in Neurobiology.

[35]  A. Engel,et al.  Selective Modulation of Interhemispheric Functional Connectivity by HD-tACS Shapes Perception , 2014, PLoS biology.

[36]  R. Knight,et al.  Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks , 2010, Front. Hum. Neurosci..

[37]  Philipp Sterzer,et al.  Responses of extrastriate cortex to switching perception of ambiguous visual motion stimuli , 2003, Neuroreport.

[38]  Edwin van Dellen,et al.  Structural degree predicts functional network connectivity: A multimodal resting-state fMRI and MEG study , 2014, NeuroImage.

[39]  Mark W. Woolrich,et al.  Measuring temporal, spectral and spatial changes in electrophysiological brain network connectivity , 2014, NeuroImage.

[40]  Rainer Goebel,et al.  Activity patterns in human motion sensitive areas depend on the interpretation of global motion , 2001, NeuroImage.

[41]  Christoph S. Herrmann,et al.  BOLD signal effects of transcranial alternating current stimulation (tACS) in the alpha range: A concurrent tACS–fMRI study , 2016, NeuroImage.

[42]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[43]  C. Gerloff,et al.  Non-invasive brain stimulation in neurological diseases , 2013, Neuropharmacology.

[44]  G. Rees,et al.  The Neural Bases of Multistable Perception , 2022 .

[45]  Thomas Haarmeier,et al.  Processing of Coherent Visual Motion in Topographically Organized Visual Areas in Human Cerebral Cortex , 2012, Brain Topography.

[46]  P. König,et al.  Natural scene evoked population dynamics across cat primary visual cortex captured with voltage-sensitive dye imaging. , 2011, Cerebral cortex.

[47]  Andreas K. Engel,et al.  Different coupling modes mediate cortical cross-frequency interactions , 2015, NeuroImage.

[48]  Geraint Rees,et al.  Primary visual cortex activation on the path of apparent motion is mediated by feedback from hMT+/V5 , 2006, NeuroImage.

[49]  Rolando J. Biscay-Lirio,et al.  Assessing interactions in the brain with exact low-resolution electromagnetic tomography , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[50]  A. Engel,et al.  High-frequency activity in human visual cortex is modulated by visual motion strength. , 2007, Cerebral cortex.

[51]  Andreas Bartels,et al.  Visual Motion Responses in the Posterior Cingulate Sulcus: A Comparison to V5/MT and MST , 2011, Cerebral cortex.

[52]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[53]  Michael Breakspear,et al.  Intrinsic Coupling Modes in Source-Reconstructed Electroencephalography , 2014, Brain Connect..

[54]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[55]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[56]  W. Singer,et al.  Relation between oscillatory activity and long-range synchronization in cat visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Flavio Frohlich,et al.  EEG feedback-controlled transcranial alternating current stimulation , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[58]  Robert Oostenveld,et al.  Brain symmetry and topographic analysis of lateralized event-related potentials , 2003, Clinical Neurophysiology.

[59]  Geraint Rees,et al.  Structural and functional fractionation of right superior parietal cortex in bistable perception , 2011, Current Biology.

[60]  Christoph Braun,et al.  Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS) , 2016, NeuroImage.

[61]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[62]  Andreas K. Engel,et al.  The saccadic spike artifact in MEG , 2012, NeuroImage.

[63]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[64]  Wolf Singer,et al.  Interhemispheric Connections Shape Subjective Experience of Bistable Motion , 2011, Current Biology.

[65]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[66]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[67]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[68]  W. Singer,et al.  Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[69]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[70]  I. Nelken,et al.  Response to Letter: Melloni et al., “Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades.” Neuron 58, 429–441 , 2009, Neuron.

[71]  Andrew J. Watrous,et al.  More than Spikes: Common Oscillatory Mechanisms for Content Specific Neural Representations during Perception and Memory This Review Comes from a Themed Issue on Brain Rhythms and Dynamic Coordination Sciencedirect Independent Contributions of Lfp Power and Phase to Neural Representation Content-spe , 2022 .

[72]  Andreas K. Engel,et al.  Oscillatory Synchronization in Large-Scale Cortical Networks Predicts Perception , 2011, Neuron.

[73]  Marcel van Gerven,et al.  Measuring directionality between neuronal oscillations of different frequencies , 2015, NeuroImage.

[74]  Christian Büchel,et al.  Neural Coupling Binds Visual Tokens to Moving Stimuli , 2005, The Journal of Neuroscience.

[75]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.